2030
The Journal of Experimental Biology 215, 2030-2038
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.069567
RESEARCH ARTICLE
A test of the validity of range of motion studies of fossil archosaur elbow mobility
using repeated-measures analysis and the extant phylogenetic bracket
Joel D. Hutson1,*,† and Kelda N. Hutson2
1
Department of Biological Sciences, Northern Illinois University, 1425 West Lincoln Highway, DeKalb, IL 60115-2825, USA and
2
Department of Earth Science, College of Lake County, 19351 West Washington Street, Grayslake, IL 60030-1198, USA
*Present address: Department of Biology, Elgin Community College, 1700 Spartan Drive, Elgin, IL 60123-7193, USA
†
Author for correspondence ([email protected])
SUMMARY
Recent studies have presented range of motion (ROM) data in degrees for dinosaur forelimb joints, usually via physical
manipulation of one individual. Using these data, researchers have inferred limb orientations, postures, gaits, ecological functions
and even phylogenetic trends within clades. However, important areas of concern remain unaddressed; for example, how does
ROM at a forelimb joint change after soft tissues are lost in archosaurs? And are fossil ROM methodologies amenable to
reproducibility and statistical analysis? Here, we investigated these questions using the extant phylogenetic bracket of dinosaurs.
Repeated measures of elbow joint ROM from Struthio camelus and Alligator mississippiensis forelimbs were statistically analyzed
as they were sequentially dissected through five levels of tissue removal treatment. Our data indicate that there are no statistically
significant differences in repeated measures of ROM between observers who use the same techniques. Extrinsic soft tissues,
such as integument, muscles and ligaments were found to impede ROM at the elbow joint. Intrinsic soft tissues, such as articular
cartilage, may increase ROM. The hypothesis that the articular surfaces of the bones within the elbow joints of archosaurs provide
a general approximation of mobility is supported. Final ROMs were less than the initial ROMs in both taxa, which suggests that
prior reports of elbow joint ROMs in degrees for nonavian dinosaurs may represent conservative estimates. We conclude that if
observer bias and other variables are controlled for, ROM studies of fossil archosaur limbs can obtain useful degree data for
inferring joint mobility in vivo.
Key words: range of motion, functional morphology, dinosaur, archosaur, forelimb, biomechanics, pronation, repeated measures, Crocodylia,
Struthioniformes.
Received 25 January 2012; Accepted 7 March 2012
INTRODUCTION
Study of the fossilized bones of extinct archosaurs, such as dinosaurs,
has generated a great deal of interest into their probable appearance
and habits in vivo. One way to infer what these were is to articulate
separate bony elements together to reconstruct different aspects of
the specimen. An understanding of comparative anatomy and
physiology in extant archosaurs can then be used to recreate
posture, locomotion, etc. (Abel, 1925; Nicholls and Russell, 1985).
A general knowledge of the effect that soft tissue has on individual
joint thickness and range of motion (ROM) in archosaurs would be
helpful in determining these attributes (Holliday et al., 2001), but
this is rarely quantified (Bonnan et al., 2010; Dzemski and Christian,
2007). Thus, as it is difficult or impossible to gauge the effects of
degraded soft tissue in fossilized taxa, it is often debated whether
soft tissue restricts or increases a ROM at any particular joint in
fossil archosaurs (Bennett, 1997). Likewise, it has been questioned
whether the articular surfaces of fossilized archosaur bones faithfully
represent the morphology of articular cartilage in vivo (Holliday et
al., 2001). Unfortunately, various ROM investigators may also
acknowledge that they are using methodologies that are not
conducive to repeatability (Hultkrantz, 1897; Yalden, 1966), and
rarely mention the necessity of statistically analyzing degree data,
which raises questions about the empirical validity of such studies.
Despite these concerns, the practice of physically manipulating fossil
archosaur (particularly dinosaur) forelimbs to obtain ROMs in
degrees is currently a growing area of interest. For example, direct
and indirect elbow joint ROM studies of fossil archosaur forelimbs
are important sources of phylogenetic and paleoecological data
(Hankin and Watson, 1914; Bramwell and Whitfield, 1974; Bennett,
1991; Sereno, 1993; Tereshchenko, 1994; Tereshchenko, 1996;
Carpenter and Smith, 2001; Gishlick, 2001; Carpenter, 2002;
Bonnan, 2003; Wilhite, 2003; Senter, 2005; Senter, 2006a; Senter,
2006b; Senter and Parrish, 2006; Senter and Robins, 2005; Bonnan
and Senter, 2007; Langer et al., 2007; Thompson and Holmes, 2007;
Senter, 2007; Carpenter and Wilson, 2008). To the best of our
knowledge, previous authors have not recognized that studies of
fossilized limb joint ROMs meet the requirements for a repeatedmeasures analysis, in which repeated measures between multiple
observers are statistically analyzed for significant differences. This
methodological approach offers a way of simultaneously addressing
several of the concerns raised above.
Here, the response of elbow joint ROM to a soft tissue removal
treatment was examined using the extant phylogenetic bracket (EPB)
of dinosaurs (Witmer, 1995), specifically the ostrich Struthio
camelus Linnaeus 1758 and the American alligator Alligator
mississippiensis (Daudin 1802). The dependent variable of interest
was elbow joint ROM in degrees. ROM data from shoulder, wrist
and finger joints were collected at the same time, but the results of
those experiments will be published separately. The elbow joint data
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Repeated-measures analysis of elbow mobility
are presented first here. These data were analyzed with the primary
goals of testing whether there is a significant difference in repeated
measures between observers using the same techniques, and whether
there is a significant increase or decrease in the degrees of
flexion/extension from a fully fleshed to a skeletonized elbow
(Figs1, 2). Secondary questions important to this study involved
quantitatively assessing the effect of soft tissue upon elbow ROM,
assessing whether there are statistically significant differences in
elbow joint ROM between A. mississippiensis and S. camelus,
evaluating the effect of soft tissue on pronation/supination (longaxis rotation) of the radius, and outlining the variables that can affect
the validity of reported ROMs in fossil archosaurs if they are not
controlled for.
MATERIALS AND METHODS
Experimental animals
Three frozen specimens of wild A. mississippiensis and three fresh
S. camelus wings from butchered farm animals were acquired for
the EPB study. This sample provided six available elbow joints in
the A. mississippiensis specimens, and three in the S. camelus
specimens. The A. mississippiensis specimens were juvenile females
with lengths of 137, 127 and 102cm. The left forelimb of the 137cm
A. mississippiensis specimen was observed to be damaged upon
delivery, which did not appear to affect ROM. The S. camelus
specimens were from domesticated male and female yearlings of
adult size (Cooper, 2005). The male provided right and left wings,
and the female a right wing. Alligator mississippiensis specimens
were examined immediately after being thawed, and all specimens
were kept refrigerated for the duration of the study once
measurements started. Measurements were taken in 2007 at Northern
Illinois University. The skeletonized limbs were donated to the
Biology Department Museum of Northern Illinois University.
Collection of repeated-measures data
Observers one and two (J.D.H. and K.N.H.) each repeatedly
measured the elbow flexion/extension ROMs three times over five
levels of sequential soft tissue dissection treatments: (1) ROM1 –
all soft tissues, including full integument (i.e. skin, scales and
feathers) remain attached; (2) ROM2 – integument is removed; (3)
ROM3 – muscle bellies and their associated tendons are removed;
(4) ROM4 – synovial joint capsules and ligaments are removed;
and (5) ROM5 – articular cartilage is removed until no soft tissue
remains on the bones (i.e. skeletonized to emulate fossilized
archosaur bones).
Each treatment level and accompanying repeated measures were
separated by 1day of refrigeration while soft tissue was removed.
Soft tissue was removed in ROM2–ROM4 with a scalpel and
forceps. In ROM5, the articular cartilage was removed by soaking
in a potassium hydroxide (KOH) solution at 60–70°C, with mild
scraping as needed. The tissue was dissected away faster than it
could decay, and all forelimbs were kept moist throughout the
dissections and repeated measures.
Before collecting ROM data, we examined and practiced with
two juvenile A. mississippiensis specimens and three adult S.
camelus wings that had been obtained earlier from the same
sources. One forelimb of each species was skeletonized so that we
could conduct blind (i.e. without having any experience of the effect
of soft tissues) ROM5 trials in imitation of researchers who are
forced by necessity to do the same with fossilized archosaur limb
elements. We then dissected the other specimens that we had
obtained earlier, and trained together to collect data in as similar a
manner as possible during each treatment level using an inclinometer
ROM1
2031
ROM5
Starting point of
extension
Humerus
Ulna
Radius
Fig.1. A skeletonized left forelimb of Alligator mississippiensis in postaxial
(medial) view, showing a stylized comparison between total ROM1
(94.5deg) and total ROM5 (46.4deg) means of elbow joint flexion and
extension. This figure and the next have arbitrary starting points of
extension, and are depicted primarily to illustrate the comparative
difference in degrees between fully fleshed and bone-on-bone ROMs,
which has important implications for fossil archosaur range of motion
(ROM) studies. The radial piston mechanism and wrist folding are not
depicted here.
(Model AF-P34214, Pinball Magic, Green Bay, WI, USA) accurate
to 0.5deg.
Repeated measures in degrees of elbow joint ROM were taken
in a standardized fashion for each specimen. The inclinometer was
pressed or positioned parallel to the long axis of a long limb bone
for each degree measurement. All ROM measurements were
obtained by moving the limb elements in as close to a vertical plane
as possible, because the inclinometer required gravity to operate. It
must be noted that tetrapod elbow joints are never perfectly planar
hinges (Cuénod, 1888; Yalden, 1966), and so positioning the
forearm to flex and extend vertically did not remove the effects of
a slight long axis rotation of the forearm into pronation (inwards
and forwards). However, this method was required for the
inclinometer to operate effectively.
For the first three treatment levels, which still had attached soft
tissue that was extrinsic to the elbow joint, the S. camelus humeri
(upper arm bones) were physically held immobile with one hand.
The humeri were held at an obtuse angle that allowed gravity to
flex and extend the forearm. The A. mississippiensis humeri were
immobilized in the same manner, but their smaller forearms were
physically flexed and extended until firm resistance was met. For
ROM4 and ROM5, all humeri were immobilized in blocks of
modeling clay and held in place by one observer to allow the
observer manipulating the specimen to articulate and move the radius
and ulna (forearm bones; Figs1, 2) with both hands. The radii and
ulnae were then flexed and extended until their proximal articular
surfaces disarticulated from each other or the humerus, or when the
bones collided. The observer who was not physically manipulating
the forelimbs recorded the degree measurements, but did not allow
the first observer to see them until all measurements were finished,
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2032 The Journal of Experimental Biology 215 (12)
variables were encountered that can potentially introduce a large
amount of variability when measuring elbow joint ROM.
ROM1
DISCUSSION
Significant treatment, observer and species interactions
ROM5
Humerus
Ulna
Radius
Starting
point of
extension
Fig.2. A skeletonized left forelimb of Struthio camelus in postaxial (medial)
view, showing a stylized comparison between total ROM1 (129.7deg) and
total ROM5 (103.3deg) means of elbow joint flexion and extension. The
radial piston mechanism and wrist folding are not depicted here.
and the order of data gathering was alternated with each set of
measurements to control for observer bias.
Statistical analyses
Preliminary analyses based on a repeated-measures ANOVA
revealed that handedness was not a significant factor affecting ROM
within A. mississippiensis elbow joints. Three A. mississippiensis
forelimbs were then chosen using a random number table (Zar, 1999)
to test against the three S. camelus forelimbs. A univariate repeatedmeasures ANOVA was used to compare ROM of the two species:
species was the between-subject factor (two levels), with treatment
(five levels), observer (two levels) and repeated measures (i.e. time;
three levels) as the three within-subject factors. The analysis was
performed in STATISTICA® (StatSoft, Tulsa, OK, USA), which
provided a conservative Greenhouse–Geisser and a more liberal
Huynh–Feldt adjustment to the P-values to account for the
correlation between repeated measures on the same subjects (von
Ende, 2001).
RESULTS
Our data show that there were no statistically significant differences
in the repeated measures taken by both observers using the same
techniques. In contrast, the effect of the five levels of dissection
treatment was statistically significant. Therefore, the effect of soft
tissue on elbow joint ROM was successfully quantified. The ROMs
of fully fleshed elbow joints in both species were found to be greater
than that of the same joints when skeletonized to emulate the
fossilized bones manipulated in ROM studies of dinosaur forelimbs.
These data thus show that ROM studies of fossil archosaur elbow
ROMs may underestimate in vivo ROM, provided that their
techniques are similar to those used in this study. When differences
in ROM are accounted for, the S. camelus specimens were found
to have higher elbow joint ROMs than the A. mississippiensis
specimens. The data also reveal that soft tissue affects elbow joint
ROM in two ways. Soft tissue extrinsic to the joint inhibits ROM,
whereas soft tissue intrinsic to the joint may have the opposite effect.
Both types of soft tissue prohibit long-axis rotation of the forearm
bones into pronation or supination at the elbow joint. Numerous
The ROMs in degrees of the A. mississippiensis and S. camelus
elbows, as estimated by different observers across increased levels
of tissue removal (Table1), were analyzed as a repeated-measures
design. The three-way interaction of species ⫻ treatment ⫻ observer
was only marginally significant, given the disparity between the
more liberal Huynh–Feldt adjustment (P0.026) and the more
conservative Greenhouse-Geisser adjustment for sphericity
(P0.065; Table2). The basis for the interaction appears to be the
increased ROM3 in A. mississippiensis as compared with S. camelus
(Fig.3), as well as the significantly lower ROM2 estimate by
observer two for A. mississippiensis (Fig.4). However, both the
treatment ⫻ species (Greenhouse–Geisser, P0.001) and treatment
⫻ observer (Greenhouse–Geisser, P0.005) two-way interactions
were significant. In the case of the former (Fig.3), even when
averaged across observers, the estimated ROM generally was
greater for S. camelus than A. mississippiensis, with the exception
of ROM3. For the treatment ⫻ observer interaction, observer two
estimates of ROM were significantly less for ROM2, which probably
accounts for the major difference in the two response curves (Fig.5).
The lack of a significant difference in overall ROMs for each
species per observer is noteworthy (Table2, Fig.5). This shows that
not only did each observer consistently obtain similar ROM
measurements, but their overall ROMs were not significantly
different for the two species. This indicates that the observer’s
combined measurements were not significantly different overall, and
were particularly consistent with S. camelus. This may reflect the
initial training and practicing on specimens beforehand, extensive
efforts to make sure that the degree data for replicate measurements
were obtained in the same manner, as well as the decision to use
gravity as a uniform application of force for ROM1–ROM3 on S.
camelus (discussed further below).
The larger variance, as shown by error bars, in replicate
measurements for ROM1 is best explained by the observation that
those measurements involved the greatest amount of impeding
extrinsic soft tissue (Fig.5). Despite training and practice, even tiny
variations in angle (S. camelus) and force applied (A.
mississippiensis) as a result of the presences of scales, skin folds
and feathers, likely caused the largest range of reported ROMs.
ROM2 exhibited the smallest variance in measurements (Fig.3).
The small variance in ROM2 is believed to have been caused by a
tightly constrained motion brought about by the muscles and
tendons, which surround and stabilize joints, and a lack of impeding
integument that could produce large variations in how the forearm
flexed or extended. By contrast, the removal of restrictive muscles
and tendons in ROM3 considerably loosened all connections
between bones.
Observers one and two did not exhibit similar slopes for replicate
measurements made between ROM1 and ROM2 for A.
mississippiensis (Fig.4). The observers trained beforehand to apply
a uniform force to the A. mississippiensis elbows throughout
ROM1–ROM3, but the positive slope by observer one and the
negative slope by observer two between ROM1 and ROM2 indicate
that observer two exerted less force than in ROM1 (hence the
decreased ROM plotted). Otherwise, if the same force had been
applied, the loss of impeding musculature should have increased
the ROM, as occurred with observer one. A return to similar replicate
measurements in ROM3 by both observers likely reflects the
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Repeated-measures analysis of elbow mobility
2033
Table1. Repeated measures of elbow joint flexion/extension across five dissection treatments (ROM1–ROM5) upon the experimental
animals
Flexion/extension (deg)
Species
Joint
Alligator mississippiensis
Observer
Left elbow (137cm)
1
2
1
2
1
2
1
2
1
2
1
2
Left elbow (102cm)
Right elbow (137cm)
Struthio camelus
Right elbow (么)
Left elbow (么)
Right elbow (乆)
ROM1
79
114
83
90
106
103
135
132
105
109
140
144
88
100
90
78
109
103
138
135
98
116
146
145
ROM2
80
101
97
73
103
104
140
146
105
119
133
149
looseness of the joint at this stage of dissection, and the lack of
impeding integument and musculature. This lack of restrictive soft
tissue likely caused more variance in replicate measurements,
regardless of differences in applied force.
The overall increase in ROM between ROM1 and ROM3 in A.
mississippiensis reflected our initial decision to physically move the
A. mississippiensis forearms until firm resistance was met. This
produced a ROM pattern whereby the steady removal of soft tissue
from ROM1 to ROM3 produced looser articulations and less extrinsic
soft tissue to physically impede flexion and extension (Fig.3). This
process culminated in ROM3, wherein both observers indirectly
observed that the loose joint capsule around the A. mississippiensis
elbow joint was allowing the forearm to dislocate. The tighter joint
capsule of S. camelus resisted this dislocation, although this only
partially explains why this species did not exhibit an increase in ROM
from ROM1 to ROM3 (Fig.3). We do not know whether the loose
joint capsules of A. mississippiensis were the result of the specimens
136
65
108
75
105
63
120
122
130
106
127
112
120
70
117
69
135
70
125
121
118
112
115
107
ROM3
122
65
122
70
136
80
122
119
120
111
122
110
175
144
159
152
155
146
120
105
113
117
115
74
170
159
160
149
154
140
125
111
113
117
111
72
ROM4
174
146
153
150
152
140
120
105
116
118
112
74
63
64
74
81
59
82
82
101
92
87
110
86
65
68
70
75
54
79
82
102
86
89
107
91
ROM5
67
70
65
83
56
80
96
103
93
88
103
86
39
43
40
59
50
40
101
98
83
126
88
123
43
50
41
56
47
41
96
100
81
136
92
128
38
47
45
56
53
47
92
96
77
128
98
116
being juveniles. The literature suggests that aerial and aquatic flapping
amniotes (land-dwelling tetrapods) have tight joint capsules with
ligaments to resist the bending and/or torsional stresses of leading
edge streams and flapping (Norberg, 1970; Clark and Bemis, 1979;
Vazquez, 1992; Vazquez, 1994; Prondvai and Hone, 2008). Struthio
camelus is descended from aerial avians, and may have retained a
tight elbow joint capsule. Alligator mississippiensis, though semiaquatic, does not use its forelimbs to ‘fly’ underwater, or to paddle
(Meers, 1999), which suggests that it does not need a comparably
rigid elbow joint area. The observation that the radial and ulnar
articulations with the humerus are not aligned in the plane of elbow
joint flexion and extension, with one on top of the other, as in many
other tetrapods with stiff elbow joints, supports this assumption
(Martins, 1862; Alix, 1863; Alix, 1874; Hultkrantz, 1897; Parsons,
1899; Vialleton, 1924; Savage, 1957).
The negative slope of the S. camelus replicate measurements
exhibited little change between ROM1 and ROM5 (Fig.4). This
Table2. Greenhouse–Geisser and Huynh–Feldt adjusted output from STATISTICA® of univariate repeated-measures ANOVA
Greenhouse–Geisser
Treatment
Treatment ⫻ Species
Error
Observer
Observer ⫻ Species
Error
RM
RM ⫻ Species
Error
Treatment ⫻ Observer
Treatment ⫻ Observer ⫻ Species
Error
Treatment ⫻ RM
Treatment ⫻ RM ⫻ Species
Error
Observer ⫻ RM
Observer ⫻ RM ⫻ Species
Error
Treatment ⫻ Observer ⫻ RM
Treatment ⫻ Observer ⫻ RM ⫻ Species
Error
Huynh–Feldt
d.f.
F
P
Adj. d.f. 1
Adj. d.f. 2
Adj. P
Adj. d.f. 1
Adj. d.f. 2
Adj. P
4
4
16
1
1
4
2
2
8
4
4
16
8
8
32
2
2
8
8
8
32
37.262
26.572
0.000000
0.000001
1.604
1.604
6.41670
6.41670
0.000380
0.000999
3.183
3.183
12.731
12.731
0.000001
0.000008
2.715
4.353
0.175
0.105
1.000
1.000
4.000
4.000
0.175
0.105
1.000
1.000
4.000
4.000
0.175
0.105
0.317
0.017
0.737
0.983
1.508
1.508
6.033
6.033
0.682
0.960
2.000
2.000
8.000
8.000
0.737
0.983
9.843
3.689
0.000325
0.026
2.209
2.209
8.836
8.836
0.005
0.065
4.000
4.000
16.000
16.000
0.000325
0.026
0.410
1.378
0.907
0.243
1.935
1.935
7.740
7.740
0.671
0.306
4.654
4.654
18.615
18.615
0.825
0.278
0.117
2.146
0.891
0.179
1.167
1.167
4.668
4.668
0.784
0.210
1.766
1.766
7.063
7.063
0.869
0.188
0.552
1.302
0.808
0.277
2.971
2.971
11.885
11.885
0.655
0.319
8.000
8.000
32.000
32.000
0.808
0.278
RM, repeated measures.
Significant P-values are in bold.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2034 The Journal of Experimental Biology 215 (12)
220
Alligator
mississippiensis
Flexion/extension (deg)
200
Struthio
camelus
180
160
140
120
100
80
60
40
20
0
ROM1
ROM2
ROM3
ROM4
ROM5
Fig.3. Effect of five sequential levels of dissection treatment on the
separate repeated measures of A. mississippiensis and S. camelus elbow
joint ROMs. Error bars indicate the variance (95% confidence intervals) of
degree measurements for this and following figures. Note that the ROM
slopes of both species do not coincide, nor do they follow the same pattern
throughout the five levels. The ROM slope of A. mississippiensis is not
linear. The five treatment levels had less of an effect on the S. camelus
ROMs than the A. mississippiensis ROMs, although the overall trend in
ROM was downward from ROM1 to ROM5 in both species.
indicates that there was less treatment effect on the S. camelus elbow
ROM than in A. mississippiensis. In hindsight, the steady decrease
in S. camelus ROMs can be explained by our initial decision to use
gravity as the constant source of force to extend the S. camelus
forearms for ROM1–ROM3. Although this decision created a more
uniform and therefore repeatable application of force, it created an
unforeseen problem. In contrast to the A. mississippiensis specimens,
the use of gravity to apply force caused S. camelus replicate
measurements to decrease from ROM1 to ROM3. The S. camelus
forearms steadily weighed less as tissue was dissected away, which
progressively exerted less force upon the elbow joint, causing the
forearm to extend less. However, weight loss does not completely
explain why these replicate measurements did not increase. That
discrepancy may be because the joint capsules around the elbow
joints of S. camelus were observed to be much tighter than those
in A. mississippiensis, particularly in the ulnar and radial collateral
ligaments that bracket the elbow joint. This tightness may have
caused a steadily increasing restriction in ROM in the first three
treatment levels as soft tissue mass was taken away. Thus, the
220
200
A
Flexion/extension (deg)
180
B
techniques we initially decided upon did produce significantly
different ROM patterns in both species for ROM1–ROM3.
The decrease in elbow ROMs for both species for ROM4 and
ROM5 relative to ROM1 was partially the result of an initial
observation that the forearms could not completely extend to the
180deg value in ROM1 (Fig.3). We therefore made the decision
to treat their elbows as joints that did not completely dislocate to
produce natural movements (e.g. Yalden, 1966). This of course did
not prevent the elbows from dislocating in ROM3 for A.
mississippiensis, in which we could not see the articular cartilage
because of the opaque joint capsule. However, we did apply this
knowledge to ROM4 and ROM5. As detailed in the Materials and
methods, we physically moved the forearm elements in the last two
levels, but stopped flexion or extension immediately upon visual
disarticulation of the elements, similar to reported methodologies
in recent dinosaur forelimb ROM publications (e.g. Carpenter,
2002). For ROM4 in S. camelus, the endpoint of flexion was
measured when the ulna completely disarticulated from the humerus,
but with the radius in full articular contact with the humerus.
Similarly, flexion during ROM5 in A. mississippiensis produced
dislocation of the ulna from the humerus, but not the radius, which
stayed in firm articulation with the humerus until it impacted in the
radial fossa (humeral depression). Unlike the first three treatment
levels, in which force was applied to the forearms perpendicular to
the radial and ulnar diaphyses (shafts), in ROM4–ROM5 the
observers pressed the forearms directly onto the humeral condyles.
If the forearms had dislocated in ROM1–ROM3, one could not have
observed this state visually because of the overlying soft tissue, but
this state was inferred in ROM3. These observations combine to
suggest that increased ROMs in levels prior to ROM4 and ROM5
in A. mississippiensis may have been partially due to decreased
tension and obstruction from surrounding soft tissues, and perhaps
associated dislocation within the elbow joint.
The effect of soft tissue on elbow ROM in S. camelus and
A. mississippiensis
A major motive for undertaking this study was to quantitatively
examine the question of whether soft tissue increased or decreased
elbow joint ROM from ROM1 to ROM5 in A. mississippiensis and
S. camelus. Similar research has been performed on domesticated
animals to determine the effects of soft tissue on ROM. For example,
Kolwe (Kolwe, 1920) and Roos et al. (Roos et al., 1992) have
undertaken and summarized veterinary research measuring how the
ROM of pronation and supination in cats and dogs may increase as
Observer 1
Observer 2
160
140
120
100
Fig.4. Effect of the interaction between treatment (five sequential
levels), species and observer on the separate repeated measures of
(A) A. mississippiensis and (B) S. camelus elbow joint ROMs. Note
that observer twoʼs repeated measures were significantly lower for
A. mississippiensis in ROM2, but were significantly higher for ROM5
in S. camelus. Both observers were responsible for the nonlinear
trend in A. mississippiensis repeated measures.
80
60
40
20
0
–20
ROM2
ROM4
ROM1
ROM3
ROM5
ROM2
ROM4
ROM1
ROM3
ROM5
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Repeated-measures analysis of elbow mobility
Flexion/extension (deg)
180
Observer 1
160
Observer 2
140
120
100
80
60
40
ROM1
ROM2
ROM3
ROM4
ROM5
Fig.5. Effect of the interaction between treatment (five sequential levels)
and observer on the combined repeated measures of A. mississippiensis
and S. camelus elbow joint ROMs. The slope of the lines indicates that the
treatment factor had a significant effect on replicate measurements for both
observers and that the observers differed significantly in their repeated
measures for ROM2.
soft tissue (i.e. extrinsic tissue) is sequentially dissected away from
the elbow to the wrist joint. Other researchers have noted that soft
tissue impedes ROM in monitor lizards (Tereshchenko, 1994), and
that muscle tonus serves to restrict limb joint ROM in vivo in
comparison to dead specimens because of tension (Hultkrantz,
1897). The question of interest here relates to whether it is possible
to use EPB results (Witmer, 1995) to extrapolate back to in vivo
ROMs in fossil archosaurs. For example, Dzemski and Christian
(Dzemski and Christian, 2007) sequentially dissected soft tissue
away from S. camelus cervical vertebrae and measured ROMs in
order to reanalyze how sauropodomorph dinosaur necks could have
moved in vivo. That question was analogous to this study, but
involved vertebral rather than limb joints, limiting its comparative
value to our data, particularly as they did not find any significant
values. However, Dzemski and Christian did state that soft tissue
(we assume extrinsic) acted to restrict ROMs to a minor degree in
S. camelus, and other bird cervical vertebrae. We observed that the
scales and muscle bellies of A. mississippiensis restricted ROM by
preventing the forearm from completely flexing.
Some qualitative reports in the literature claim that some types
of soft tissue act to increase ROM at limb joints, supposedly because
of enlarged articular cartilage in comparison to the corresponding
bony surface beneath (Hay, 1911; Yalden, 1966; Shubin et al., 2006).
Other authors have raised concerns that the articular cartilage of
archosaurs does not faithfully represent the articular morphology
of the bone underneath it (Holliday et al., 2001), as it does with
therian mammals (marsupials and placentals) (Bonnan and Senter,
2007). Here, we confirmed that the forelimb bones of both A.
mississippiensis and S. camelus do not articulate as precisely (in a
resting position) as they do when covered with articular cartilage.
This condition is most problematic in the wrist and elbow joints.
In particular, the skeletonized ulnae of both species do not articulate
precisely between the ulnar and radial condyles of the humerus.
When articulated with the humerus in isolation, a skeletonized ulna
has a different resting position than the resting position of the
isolateral (from the same side of the body) radius would indicate.
During ROM5 measurements, we usually moved the radius and ulna
while they were articulating (touching), although this tended to
disarticulate the radius from the radial condyle of the humerus.
Moving the radius to the radial condyle of the humerus slightly
2035
disarticulated the radius from the ulna, although they did not lose
contact. Moreover, articulating the distal ends of the radius and ulna
placed the proximal end of the radius where it would articulate with
the radial condyle, but slightly disarticulated from the proximal end
of the ulna. These problems illustrated the lost influence of a layer
of articular cartilage both proximally and distally. Approximately
5mm of articular cartilage was found to separate the proximal and
distal ends of the forearm bones of A. mississippiensis (radial plus
ulnar cartilage). The S. camelus specimens had less cartilage
(1–2mm), a difference that may have reflected the juvenile status
of the A. mississippiensis specimens, or other factors. We considered,
but rejected, applying modeling clay between the defleshed ROM5
bones to correct for the observed discordance in articulation (see
Gishlick, 2001). We felt that attempting bone-on-bone ROMs more
faithfully imitated the ROMs that fossil archosaur forelimb ROM
studies attempt, which do not have a firm estimate of articular
cartilage thickness. However, the bony articular surfaces of both A.
mississippiensis and S. camelus retained enough morphological
fidelity that we were able to articulate and move skeletonized limb
elements.
Lastly, another problem in the elbow of A. mississippiensis was
that the articular surfaces of the ulnar and radial condyles of the
humerus extend just as far flexad (i.e. forwards) and extensad (i.e.
behind) in ROM5, which would indicate visually that the forearm
could hyperextend. We knew that they could not, however, because
A. mississippiensis possesses a small cartilaginous olecranon process
(elbow) that prevented hyperextension in ROM4. A ROM study
with fossil archosaur forelimbs would not be able to determine this.
These difficulties illustrated the lost effect of the articular cartilage
that separated the proximal ends of the forearm bones in vivo, which
our data suggest may cause fossil archosaur forelimb ROM studies
to underestimate in vivo elbow joint ROM, provided that these
studies follow our methods.
For the elbow, the general decrease in ROMs from ROM4 to
ROM5 in A. mississippiensis, and for observer one in S. camelus,
supports the assumption that articular cartilage may increase ROM
(Fig.4). Here, we did not observe any substantial effect on ROM
or articular surface morphology during data collection between
ROM4 and ROM5, except to note that the loss of articular cartilage
made it much more difficult to articulate and move forelimb bones.
However, the power of this study is low because of the limited
sample size (N3) for the S. camelus elbow replicates. Regardless,
our data provide quantitative support (in a form other than that of
geometric morphometric measurements) for previous claims that
the articular surfaces of fossilized archosaur bones approximate the
morphology of the articular cartilage in vivo (Carpenter, 2002;
Bonnan and Senter, 2007; Bonnan et al., 2010). Regardless, further
quantitative study is required to determine whether the ratio of area
lost is equal in both articular surfaces (Tereshchenko, 1994).
Elbow joint dislocation: implications for locomotion,
pronation/supination and the radial piston mechanism in
extinct archosaurs
The topic of how far a joint can move, or dislocate without causing
permanent damage, is important in several areas of research on fossil
tetrapods. In this study we attempted to address whether dislocation
of the forearm elements with each other, or with the elbow, could
routinely contribute to locomotion, pronation/supination and the
radial piston mechanism (proximodistal sliding of the radius during
flexion and extension). In regard to the incidence of dislocation (i.e.
that does not cause permanent damage), Yalden (Yalden, 1966)
extensively described how many extant therians have carpal joints
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2036 The Journal of Experimental Biology 215 (12)
that routinely dislocate past the limits of their articular surfaces.
This type of innocuous dislocation during flexion and extension was
not observed in A. mississippiensis and S. camelus elbows during
ROM1, and X-rays taken of the joints in extremes of flexion and
extension did not indicate that any dislocation was occurring.
Moreover, prior experimentation had shown that the fully fleshed
forearms of both species would not extend to 180deg, nor flex
completely unless by dislocation. This dislocation could not have
been forced without damaging the specimens. Researchers who
study the elbow ROM of dinosaurs may not know this unless they
also utilize the EPB (Carpenter, 2002; Bonnan and Senter, 2007).
This information indicates that dislocation of the elbow joint does
not normally contribute to locomotion in A. mississippiensis or
idiomotion (limb movements other than for locomotion) in S.
camelus.
The topic of harmless joint dislocation is also important in debates
on whether the first aerial amniotes (pterosaurs) walked terrestrially
using quadrupedalism or bipedalism. The relevant question is
whether the articular surface of the proximal femoral (thigh bone)
head could have moved past the extent of the articular surface in
the hip joint (Unwin, 1988; Bennett, 1997). We will postpone a
more detailed discussion of this topic until the results of our shoulder
joint ROM study are published. However, this question was
important to test here in the elbows of the EPB of dinosaurs. It is
sometimes assumed that many tetrapod forearms can partially
dislocate their proximal articulations from their respective humeral
condyles during locomotion to physically pronate and supinate their
forearm elements (Hultkrantz, 1897; Gasc, 1963). Moreover, until
a recent series of refuting evidence from ROM studies performed
with dinosaur forelimbs (Sereno, 1993; Carpenter and Smith, 2001;
Carpenter, 2002; Bonnan and Senter, 2007), it had often been
assumed that some dinosaurs could freely pronate and supinate their
radii like therian mammals.
The radii and ulnae of the EPB specimens in this study were
prevented from leaving the extensor articular surfaces of their
humeral condyles because the joint capsule ended proximal to the
limits of these articular surfaces, which firmly bound the entire area.
The radii and ulnae were also observed to be tightly bound by
radioulnar ligaments common to other tetrapods, albeit more loosely
in A. mississippiensis, and this tension prevented long-axis rotation
of either element in relation to the distal humerus, or to each other.
One A. mississippiensis elbow joint was sacrificed prior to this study
to observe forced axial rotation of the radius to a full 180deg of
pronation. This experiment resulted in permanent dislocation of the
radius from the radial notch and the elbow via torn radioulnar and
collateral ligaments, particularly surrounding the elbow joint.
Enlarged cartilaginous articular edges also expanded the sizes of
the intercondylar ridges in each taxon, further restricting motion to
conjoint flexion and extension. However, a small amount of
proximodistal sliding of the radius (i.e. the radial piston mechanism)
was possible relative to the ulnar shaft.
The radial piston mechanism reported among many tetrapods was
observable in both A. mississippiensis and S. camelus (Gegenbaur,
1864; Fürbringer, 1886; Rabl, 1910) and had to be accounted for
as the ROMs in degrees were measured. As the elbows were flexed,
the change in depth of the radial condyle and the presence of an
ulnar expansion extensad to the radius partially caused the radius
to slide distally and linearly along the ulna. Connective soft tissues
served to amplify and guide this effect as well. The opposite effect
was observed during extension. The distal radius pushed on the wrist
and caused it to deviate in the ulnar direction upon elbow flexion
and vice versa for elbow extension. The radial piston mechanism
did appear to increase the ROM of the elbow joints slightly by
pushing the radius distally out of the way during flexion, which had
the effect of delaying impaction of the radius between the ulna and
humerus. However, dislocation of the radius from the ulna or radial
condyle was not observed during ROM1 or ROM2, although in
ROM3 for A. mississippiensis the loosened joint capsule allowed
the forearm to dislocate slightly in every direction. Thus, our
investigations of individual forearm element and elbow joint
dislocation show that the extrinsic soft tissues in the experimental
animal elbow joints combine to resist disarticulation.
ROM study methodologies and reproducibility
A carefully controlled analysis with repeated measures was chosen
for this EPB experiment because the measuring of the ROMs of
limb joints meets the criteria of introducing a potentially large
amount of variability and observer bias (von Ende, 2001). Moreover,
we were interested in how the elbow ROMs changed between
successive levels of treatment. There were many variables that
needed to be controlled for to obtain ROM data that could be
statistically analyzed. For example, the methods of overlaying
pictures of limb segments that had moved, or measuring ROM from
a computer screen or overhead projector with a protractor or
goniometer, were found to be inaccurate because the elbow is never
a uniplanar hinge in tetrapods (Cuénod, 1888; Yalden, 1966). Thus,
the forearm will slant either inwards or outwards during flexion, as
well as rotate about its long axis. All of these attempts introduced
an unacceptable amount of parallax. The method of finding the exact
vertex of joint movement, and inserting a screw or pin to aid in the
use of a protractor or goniometer (Yalden, 1966), was also found
to be impractical because this point was often dissected away, and
the small A. mississippiensis bones were susceptible to fracturing
during pin insertion. Overall, the inclinometer was found to be the
most accurate instrument and the easiest to use, if used correctly.
If the element in motion was oriented to move vertically to reduce
the effects of circumduction (i.e. a curving path of flexion and
extension), the inclinometer could be placed upon any point without
any further requirements. Thus, inclinometer measurements were
found to change only with variations in how the observer
manipulated the specimen.
Other variables that needed to be controlled were those associated
with observer bias. The most important bias was experience, which
we attempted to equalize by training together on the same specimens.
Moreover, we initially found that once we knew what the ROM
was in degrees for a joint, we would try to equal or exceed it the
next time we measured it. It was assumed that hiding the
measurements from the observer manipulating the specimen, by
having a second observer gather degree data, would preclude this
bias and result in a more consistent application of force and
technique. In regard to our secondary questions concerning the
methodology used in ROM on fossil archosaurs, the results above
suggest that an inclusion of methodology into the discussions of
fossil archosaur ROMs is essential. Even seemingly unimportant
differences in methodology produce different ROMs.
Our results do not shed light on whether the direct method of
obtaining joint ROMs is more accurate than indirect methods, such
as those that mathematically estimate ROM from the articular surfaces
of bones (Hultkrantz, 1897; Tereshchenko, 1994; Tereshchenko,
1996). A comparative test on this material would have to be
undertaken to resolve this. Otherwise, we feel that our methodology
compares favorably with other repeatable ROM techniques in use
(Yalden, 1966), provided that more than one observer is on hand to
repeat the measurements. The large amount of observer bias dictates
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Repeated-measures analysis of elbow mobility
that a repeated-measures statistical analysis is the method of choice
for researchers who plan on basing important physiological inferences
on ROM data taken from fossil bones.
Extrinsic versus intrinsic joint soft tissues
Based on the nonlinear A. mississippiensis trend and the observation
that ROM1 elbow flexion and extension did not rely on habitual
separation of complementary articular surfaces in either species, the
five treatment levels used in the present study need to be split into
two segments. The nonlinear trend of the A. mississippiensis ROMs
is due to the application of a uniform physical force in the first three
levels. The data show an upward trend for the first three, but a
downward trend for the last two levels (Fig.3). These opposing
slopes reflect the observation that data from ROM1–ROM3 came
from an applied force as soft tissue extrinsic to the joint was
removed, whereas data from ROM4 and ROM5 came from changes
in area in articular surfaces after articular cartilage was removed,
and hence had nothing to do with applied force. Therefore,
ROM1–ROM3 measure a different change in ROM than ROM4
and ROM5 because the role of the soft tissues involved is different.
The first three treatment levels examine the effect of soft tissue
extrinsic to the elbow joint. As this soft tissue was removed, the ROM
increased for A. mississippiensis as long as the applied force stayed
the same. This was because soft tissue that physically impeded ROM,
such as the volume of muscle bellies, prevented the joints from fully
flexing or extending. Unlike in A. mississippiensis, the initial decision
to use the force of gravity for levels one to three in S. camelus resulted
in an unforeseen decrease in force as mass (i.e. peripheral soft tissue)
was removed. This steady decrease in force caused the ROM to
decrease rather than increase because the opposing resistance of the
tight joint capsule did not change. If a consistent physical force had
been applied for S. camelus instead of gravity, as was done with A.
mississippiensis, we predict that the trend would have exhibited a
linear increase in ROM for ROM1–ROM3 as well. That would have
provided a more accurate picture of the differences between
ROM1–ROM3 and ROM4–ROM5.
The last two treatment levels solely examine the effect on ROM
of articular cartilage within (intrinsic to) the elbow joint. For A.
mississippiensis, a similar decrease in ROM was observed after
articular cartilage was removed for both observers (Fig.3). In other
words, the available data show that ROM1–ROM3 exhibit a linear
increase in ROM as the volume of impeding extrinsic soft tissue is
dissected away, whereas ROM4 and ROM5 show a linear decrease
in ROM as the volume and area of articular cartilage is removed. The
increased area and/or depth of articular surfaces covered by cartilage
provide a possible explanation for an increased ROM in ROM4 versus
ROM5. For S. camelus, observer one measured an overall decrease
in ROM, whereas observer two measured an overall increase. This
divergence may be the result of individual differences in visual
estimates of where the articular surfaces began and ended, despite
earlier practice. Another possibility is that the discrepancy may
represent real differences in the effect of articular cartilage on elbow
ROM. In future experiments, using a larger sample size might resolve
this dichotomy.
Ideally, the ROM of joints in vivo should have been used in this
study in place of the ROM1 of dead specimens. This could have been
attempted by immobilizing the upper arm of the juvenile A.
mississippiensis specimens and taking repeated measures of their
voluntary elbow joint ROMs. However, this methodology would have
been impractical with the much larger, and therefore more dangerous,
adult S. camelus specimens. Instead, we propose that in vivo ROMs
could be achieved using digital inclinometers strapped directly to the
2037
forearm of anesthetized or even freshly dead specimens. The desired
ROM could then be isolated by electrically stimulating the relevant
muscle or muscle groups (see Kolwe, 1920), or by simply recording
a range of repeated measures of voluntary ROMs from the specimens
over a period of time. Data from the digital inclinometer could be
relayed directly to a computer for tabulation and statistical analysis.
Then these data could be compared with a skeletonized ROM5 of
the same limb segments.
Our dissection and joint movement results suggest that if applied
force stays the same, a fully fleshed archosaur elbow joint will exhibit
an increase in flexion and extension ROM as integument, muscles
and tendons are removed. However, if only articular cartilage is
considered, we predict that the elbow joint will exhibit a decrease in
ROM if it is removed. The latter statement is the one more applicable
to ROM studies of fossil archosaurs such as dinosaurs (Figs1, 2).
Even after the increase in ROM from ROM1 to ROM3 is taken into
account, there is an overall decrease in the ROM of elbow flexion
and extension from ROM1 (fully fleshed) through ROM5 (bone-onbone) in both A. mississippiensis and S. camelus in this study. Our
data suggest that reported fossil ROMs of dinosaur elbow joints likely
underestimate the actual ROM in vivo, especially if, as in this study,
the forearm elements were moved until disarticulation was observed.
Future research is essential to test whether the effects of extrinsic
versus intrinsic soft tissue also apply on limb joints with more ROM
than the elbow joint, such as the shoulder and hip joints. Otherwise,
this study affirmed the need for more ROM studies to help reconstruct
the functional morphology of dinosaur forelimbs, as well as other
fossil archosaur limbs.
ACKNOWLEDGEMENTS
This study was conducted during the graduate research of J.D.H. at Northern
Illinois University. Practice A. mississippiensis specimens were loaned to us from
Western Illinois University, thanks to Matthew F. Bonnan. All A. mississippiensis
specimens were ultimately provided by Ruth Elsey of the Rockefeller Wildlife
Refuge (Grand Chenier, LA, USA) and the S. camelus specimens were given
freely by Mark Wiley of Freedom Sausage Inc. (Earlville, IL, USA). We are grateful
to Carl von Ende for freely providing his invaluable expertise in repeated
measures, and for the use of his statistical software. Chris Hubbard provided initial
laboratory space and equipment, and kind suggestions from Phil Senter of
Fayetteville State University and an anonymous reviewer helped improve this
manuscript.
FUNDING
This work was supported by a Jurassic Foundation Research Grant; the
Geological Society of America [grant numbers 8297-06, 8980-08]; a Northern
Illinois University Dissertation Completion Fellowship; three Northern Illinois
University Biology Departmental Graduate Research Grants (to J.D.H.), and
Northern Illinois University Presidential Scholarship funds (to J. Michael Parrish).
The authors declare no financial or competing interests.
REFERENCES
Abel, O. (1925). Geschichte und Methode der Rekonstruktion vorzeitlicher Wirbeltiere.
Jena: Gustav Fischer.
Alix, E. (1863). Mouvements de lʼavant-bras chez les oiseaux. Bull. Sci. Philom. 28,
48-51.
Alix, E. (1874). Essai sur Lʼappareil Locomoteur des Oiseaux. Paris: G. Masson.
Bennett, S. C. (1991). Morphology of the late Cretaceous pterosaur Pteranodon and
systematics of the Pterodactyloidea. PhD dissertation, University of Kansas,
Lawrence, KS.
Bennett, S. C. (1997). Terrestrial locomotion of pterosaurs: a reconstruction based on
Pteraichnus trackways. J. Vertebr. Paleontol. 17, 104-113.
Bonnan, M. F. (2003). The evolution of manus shape in sauropod dinosaurs:
implications for functional morphology, forelimb orientation, and phylogeny. J.
Vertebr. Paleontol. 23, 595-613.
Bonnan, M. F. and Senter, P. J. (2007). Were the basal sauropodomorph dinosaurs
Plateosaurus and Massospondylus habitual quadrupeds? Spec. Pap. Palaeont. 77,
139-155.
Bonnan, M. F., Sandrik, J. L., Nishiwaki, T., Wilhite, D. R., Elsey, R. M. and
Vittore, C. (2010). Calcified cartilage shape in archosaur long bones reflects
overlying joint shape in stress-bearing elements: implications for nonavian dinosaur
locomotion. Anat. Rec. 293, 2044-2055.
Bramwell, C. D. and Whitfield, G. R. (1974). Biomechanics of Pteranodon. Philos.
Trans. R. Soc. Lond. B 267, 503-581.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2038 The Journal of Experimental Biology 215 (12)
Carpenter, K. (2002). Forelimb biomechanics of nonavian theropod dinosaurs in
predation. Senckenb. Lethaia 82, 59-76.
Carpenter, K. and Smith, M. (2001). Forelimb osteology and biomechanics of
Tyrannosaurus rex. In Mesozoic Vertebrate Life (ed. D. H. Tanke and K. Carpenter),
pp. 90-116. Bloomington, IN: Indiana University Press.
Carpenter, K. and Wilson, Y. (2008). A new species of Camptosaurus (Ornithopoda:
Dinosauria) from the Morrison Formation (Upper Jurassic) of Dinosaur National
Monument, Utah, and a biomechanical analysis of its forelimb. Ann. Carnegie Mus.
76, 227-263.
Clark, B. D. and Bemis, W. (1979). Kinematics of swimming of penguins at the Detroit
Zoo. J. Zool. 188, 411-428.
Cooper, R. G. (2005). Growth in the ostrich (Struthio camelus var. domesticus). Anim.
Sci. 76, 1-4.
Cuénod, A. (1888). Lʼarticulation du coude. Etude dʼanatomie comparée. Int.
Monatsschr. Anat. Physiol. 5, 385-430.
Dzemski, G. and Christian, A. (2007). Flexibility along the neck of the ostrich
(Struthio camelus) and consequences for the reconstruction of dinosaurs with
extreme neck length. J. Morphol. 268, 701-714.
Fürbringer, M. (1886). Über das Schulter und Ellbogengelenk bei Vögeln und
Reptilien. Morphol. Jahrb. 11, 118-120.
Gasc, J.-P. (1963). Adaptation à la marche arboricole chez le caméléon. Arch. Anat.
Histol. Embryol. 46, 81-115.
Gegenbaur, C. (1864). Untersuchungen zur Vergleichenden Anatomie der
Wirbelthiere. Erstes Heft. Carpus und Tarsus. Leipzig: Verlag von Wilhelm
Engelmann.
Gishlick, A. D. (2001). The function of the manus and forelimb of Deinonychus
antirrhopus and its importance for the origin of avian flight. In New Perspectives on
the Origin and Early Evolution of Birds (ed. J. Gauthier and L. F. Gall), pp. 301-318.
New Haven, CT: Yale Peabody Museum.
Hankin, E. H. and Watson, D. M. S. (1914). On the flight of pterodactyls. Aër. J. 18,
324-335.
Hay, O. P. (1911). Further observations on the pose of the sauropodous dinosaurs.
Am. Nat. 45, 398-412.
Holliday, C. M., Ridgely, R. C., Sedlmayr, J. C. and Witmer, L. M. (2001). The
articular cartilage of extant archosaur limb bones: implications for dinosaur functional
morphology and allometry. J. Vertebr. Paleontol. 21 Suppl. 3, 62A.
Hultkrantz, J. W. (1897). Das Ellenbogengelenk und seine Mechanik: Eine
Anatomische Studie. Jena: Gustav Fischer.
Kolwe, G. O. E. (1920). Über Pronation und Supination bei der Katze. Dissertation der
Tierärztlichen Hochschule zu Berlin.
Langer, M. C., Franca, M. A. G. and Gabriel, S. (2007). The pectoral girdle and
forelimb anatomy of the stem-sauropodomorph Saturnalia tupiniquim (Upper
Triassic, Brazil). Spec. Pap. Palaeontol. 77, 113-137.
Martins, C. (1862). Ostéologie comparée des articulations du coude et du genou chez
les mammifères, les oiseaux et les reptiles. Extr. Mém. Acad. Sci. Lett. Montpellier 3,
335-362.
Meers, M. B. (1999). Evolution of the crocodilian forelimb: anatomy, biomechanics,
and functional morphology. PhD dissertation, John Hopkins University, Baltimore,
MD.
Nicholls, E. L. and Russell, A. P. (1985). Structure and function of the pectoral girdle
and forelimb of Struthiomimus altus (Theropoda: Ornithomimidae). Palaeontology 28,
643-677.
Norberg, U. M. (1970). Functional osteology and myology of the wing of Plecotus
auritus Linnaeus (Chiroptera). Arkiv Zool. 22, 483-543.
Parsons, F. G. (1899). The joints of mammals compared with those of man: a course
of lectures delivered at the Royal College of Surgeons of England. J. Anat. Physiol.
34, 41-68.
Prondvai, E. and Hone, D. W. E. (2008). New models for the wing extension in
pterosaurs. Hist. Biol. 20, 237-254.
Rabl, C. (1910). Bausteine zu einer Theorie der Extremitäten der Wirbeltiere. I. Teil.
Leipzig: Verlag von Wilhelm Engelmann.
Roos, H., Brugger, S. and Rauscher, T. (1992). Über die biologische Wertigkeit der
Bewegungen in den Radioulnargelenken bei Katze und Hund. Zbl. Vet. Med. C 23,
199-205.
Savage, R. J. G. (1957). The anatomy of Potamotherium, an Oligocene latrine. Proc.
Zool. Soc. Lond. 129, 151-244.
Senter, P. J. (2005). Function in the stunted forelimbs of Mononykus olecranus
(Theropoda), a dinosaurian anteater. Paleobiology 31, 373-381.
Senter, P. J. (2006a). Forelimb function in Ornitholestes hermanni Osborn (Dinosauria,
Theropoda). Palaeontology 49, 1029-1034.
Senter, P. J. (2006b). Comparison of forelimb function between Deinonychus and
Bambiraptor (Theropoda: Dromaeosauridae). J. Vertebr. Paleontol. 26, 897-906.
Senter, P. J. (2007). Analysis of forelimb function in basal ceratopsians. J. Zool.
(London) 273, 305-314.
Senter, P. J. and Parrish, J. M. (2006). Forelimb function in the theropod dinosaur
Carnotaurus sastrei, and its behavioral implications. PaleoBios 26, 7-17.
Senter, P. J. and Robins, J. H. (2005). Range of motion in the forelimb of the
theropod dinosaur Acrocanthosaurus atokensis, and implications for predatory
behavior. J. Zool. 266, 307-318.
Sereno, P. C. (1993). The pectoral girdle and forelimb of the basal theropod
Herrerasaurus ischigualastensis. J. Vertebr. Paleontol. 13, 425-450.
Shubin, N. H., Daeschler, E. B. and Jenkins, F. A., Jr (2006). The pectoral fin of
Tiktaalik roseae and the origin of the tetrapod limb. Nature 440, 764-771.
Tereshchenko, V. S. (1994). A reconstruction of the erect posture of Protoceratops.
Paleontol. J. 28, 104-119.
Tereshchenko, V. S. (1996). A reconstruction of the locomotion of Protoceratops.
Paleontol. J. 39, 232-245.
Thompson, S. and Holmes, R. (2007). Forelimb stance and step cycle in
Chasmosaurus irvinensis (Dinosauria: Neoceratopsia). Palaeontol. Electr. 10, 1-17.
Unwin, D. M. (1988). New remains of the pterosaur Dimorphodon (Pterosauria:
Rhamphorynchoidea) and the terrestrial locomotion of early pterosaurs. Mod. Geol.
13, 57-68.
Vazquez, R. J. (1992). Functional osteology of the avian wrist and the evolution of
flapping flight. J. Morphol. 211, 259-268.
Vazquez, R. J. (1994). The automating skeletal and muscular mechanisms of the
avian wing (Aves). Zoomorphology 114, 59-71.
Vialleton, L.-M. (1924). Morphologie Générale: Membres et Ceintures des Vertébrés
Tétrapodes: Critique Morphologique du Transformisme. Paris: Librairie Octave Doin.
Von Ende, C. N. (2001). Repeated-measures analysis: growth and other timedependent measures. In Design and Analysis of Ecological Experiments, 2nd edn
(ed. S. M. Scheiner and J. Gurevitch), pp. 134-157. New York: Oxford University
Press.
Wilhite, R. (2003). Biomechanical reconstruction of the appendicular skeleton in three
North American Jurassic sauropods. PhD dissertation, Louisiana State University,
Baton Rouge, LA.
Witmer, L. M. (1995). The extant phylogenetic bracket and the importance of
reconstructing soft tissues in fossils. In Functional Morphology in Vertebrate
Paleontology (ed. J. J. Thomason), pp. 19-33. New York: Cambridge University
Press.
Yalden, D. W. (1966). A contribution to the functional morphology of the mammalian
carpus. PhD thesis, University of London.
Zar, J. H. (1999). Biostatistical Analysis, 4th edn. Upper Saddle River, NJ: Prentice
Hall.
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